An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia
Disinhibition is a core symptom of many neurodegenerative diseases, particularly frontotemporal dementia, and is a major cause of stress for caregivers. While a distinction between behavioural and cognitive disinhibition is common, an operational definition of behavioural disinhibition is still miss...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-01-01
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| Series: | NeuroImage: Clinical |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158222001449 |
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| author | Delphine Tanguy Bénédicte Batrancourt Alfonso Estudillo-Romero John S.H. Baxter Isabelle Le Ber Arabella Bouzigues Valérie Godefroy Aurélie Funkiewiez Céline Chamayou Emmanuelle Volle Dario Saracino Armelle Rametti-Lacroux Xavier Morandi Pierre Jannin Richard Levy Raffaella Migliaccio |
| author_facet | Delphine Tanguy Bénédicte Batrancourt Alfonso Estudillo-Romero John S.H. Baxter Isabelle Le Ber Arabella Bouzigues Valérie Godefroy Aurélie Funkiewiez Céline Chamayou Emmanuelle Volle Dario Saracino Armelle Rametti-Lacroux Xavier Morandi Pierre Jannin Richard Levy Raffaella Migliaccio |
| author_sort | Delphine Tanguy |
| collection | DOAJ |
| description | Disinhibition is a core symptom of many neurodegenerative diseases, particularly frontotemporal dementia, and is a major cause of stress for caregivers. While a distinction between behavioural and cognitive disinhibition is common, an operational definition of behavioural disinhibition is still missing. Furthermore, conventional assessment of behavioural disinhibition, based on questionnaires completed by the caregivers, often lacks ecological validity. Therefore, their neuroanatomical correlates are non-univocal.In the present work, we used an original behavioural approach in a semi-ecological situation to assess two specific dimensions of behavioural disinhibition: compulsivity and social disinhibition. First, we investigated disinhibition profile in patients compared to controls. Then, to validate our approach, compulsivity and social disinhibition scores were correlated with classic cognitive tests measuring disinhibition (Hayling Test) and social cognition (mini-Social cognition & Emotional Assessment). Finally, we disentangled the anatomical networks underlying these two subtypes of behavioural disinhibition, taking in account the grey (voxel-based morphometry) and white matter (diffusion tensor imaging tractography). We included 17 behavioural variant frontotemporal dementia patients and 18 healthy controls.We identified patients as more compulsive and socially disinhibited than controls. We found that behavioural metrics in the semi-ecological task were related to cognitive performance: compulsivity correlated with the Hayling test and both compulsivity and social disinhibition were associated with the emotion recognition test. Based on voxel-based morphometry and tractography, compulsivity correlated with atrophy in the bilateral orbitofrontal cortex, the right temporal region and subcortical structures, as well as with alterations of the bilateral cingulum and uncinate fasciculus, the right inferior longitudinal fasciculus and the right arcuate fasciculus. Thus, the network of regions related to compulsivity matched the “semantic appraisal” network. Social disinhibition was associated with bilateral frontal atrophy and impairments in the forceps minor, the bilateral cingulum and the left uncinate fasciculus, regions corresponding to the frontal component of the “salience” network.Summarizing, this study validates our semi-ecological approach, through the identification of two subtypes of behavioural disinhibition, and highlights different neural networks underlying compulsivity and social disinhibition. Taken together, these findings are promising for clinical practice by providing a better characterisation of inhibition disorders, promoting their detection and consequently a more adapted management of patients. |
| first_indexed | 2024-04-13T21:47:20Z |
| format | Article |
| id | doaj.art-938507977d774c37b8ff89512c599680 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-04-13T21:47:20Z |
| publishDate | 2022-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-938507977d774c37b8ff89512c5996802022-12-22T02:28:31ZengElsevierNeuroImage: Clinical2213-15822022-01-0135103079An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementiaDelphine Tanguy0Bénédicte Batrancourt1Alfonso Estudillo-Romero2John S.H. Baxter3Isabelle Le Ber4Arabella Bouzigues5Valérie Godefroy6Aurélie Funkiewiez7Céline Chamayou8Emmanuelle Volle9Dario Saracino10Armelle Rametti-Lacroux11Xavier Morandi12Pierre Jannin13Richard Levy14Raffaella Migliaccio15Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, France; Univ Rennes, CHU Rennes, Inserm, LTSI – UMR 1099, F-35000 Rennes, France; Corresponding authors at: Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Hôpital Pitié, Paris, France.Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, FranceUniv Rennes, CHU Rennes, Inserm, LTSI – UMR 1099, F-35000 Rennes, FranceUniv Rennes, CHU Rennes, Inserm, LTSI – UMR 1099, F-35000 Rennes, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, France; AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Department of Neurology, IM2A, Paris, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, FranceAP-HP, Groupe Hospitalier Pitié-Salpêtrière, Department of Neurology, IM2A, Paris, FranceAP-HP, Groupe Hospitalier Pitié-Salpêtrière, Department of Neurology, IM2A, Paris, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, France; AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Department of Neurology, IM2A, Paris, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, FranceUniv Rennes, CHU Rennes, Inserm, LTSI – UMR 1099, F-35000 Rennes, FranceUniv Rennes, CHU Rennes, Inserm, LTSI – UMR 1099, F-35000 Rennes, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, France; AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Department of Neurology, IM2A, Paris, FranceSorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Paris, France; AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Department of Neurology, IM2A, Paris, France; Corresponding authors at: Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Hôpital Pitié, Paris, France.Disinhibition is a core symptom of many neurodegenerative diseases, particularly frontotemporal dementia, and is a major cause of stress for caregivers. While a distinction between behavioural and cognitive disinhibition is common, an operational definition of behavioural disinhibition is still missing. Furthermore, conventional assessment of behavioural disinhibition, based on questionnaires completed by the caregivers, often lacks ecological validity. Therefore, their neuroanatomical correlates are non-univocal.In the present work, we used an original behavioural approach in a semi-ecological situation to assess two specific dimensions of behavioural disinhibition: compulsivity and social disinhibition. First, we investigated disinhibition profile in patients compared to controls. Then, to validate our approach, compulsivity and social disinhibition scores were correlated with classic cognitive tests measuring disinhibition (Hayling Test) and social cognition (mini-Social cognition & Emotional Assessment). Finally, we disentangled the anatomical networks underlying these two subtypes of behavioural disinhibition, taking in account the grey (voxel-based morphometry) and white matter (diffusion tensor imaging tractography). We included 17 behavioural variant frontotemporal dementia patients and 18 healthy controls.We identified patients as more compulsive and socially disinhibited than controls. We found that behavioural metrics in the semi-ecological task were related to cognitive performance: compulsivity correlated with the Hayling test and both compulsivity and social disinhibition were associated with the emotion recognition test. Based on voxel-based morphometry and tractography, compulsivity correlated with atrophy in the bilateral orbitofrontal cortex, the right temporal region and subcortical structures, as well as with alterations of the bilateral cingulum and uncinate fasciculus, the right inferior longitudinal fasciculus and the right arcuate fasciculus. Thus, the network of regions related to compulsivity matched the “semantic appraisal” network. Social disinhibition was associated with bilateral frontal atrophy and impairments in the forceps minor, the bilateral cingulum and the left uncinate fasciculus, regions corresponding to the frontal component of the “salience” network.Summarizing, this study validates our semi-ecological approach, through the identification of two subtypes of behavioural disinhibition, and highlights different neural networks underlying compulsivity and social disinhibition. Taken together, these findings are promising for clinical practice by providing a better characterisation of inhibition disorders, promoting their detection and consequently a more adapted management of patients.http://www.sciencedirect.com/science/article/pii/S2213158222001449CompulsivityDiffusion tensor imagingSemi-ecological situationSocial disinhibitionVoxel-based morphometry |
| spellingShingle | Delphine Tanguy Bénédicte Batrancourt Alfonso Estudillo-Romero John S.H. Baxter Isabelle Le Ber Arabella Bouzigues Valérie Godefroy Aurélie Funkiewiez Céline Chamayou Emmanuelle Volle Dario Saracino Armelle Rametti-Lacroux Xavier Morandi Pierre Jannin Richard Levy Raffaella Migliaccio An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia NeuroImage: Clinical Compulsivity Diffusion tensor imaging Semi-ecological situation Social disinhibition Voxel-based morphometry |
| title | An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia |
| title_full | An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia |
| title_fullStr | An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia |
| title_full_unstemmed | An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia |
| title_short | An ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia |
| title_sort | ecological approach to identify distinct neural correlates of disinhibition in frontotemporal dementia |
| topic | Compulsivity Diffusion tensor imaging Semi-ecological situation Social disinhibition Voxel-based morphometry |
| url | http://www.sciencedirect.com/science/article/pii/S2213158222001449 |
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